Research Article |
Corresponding author: Markus Koch ( markus.koch@senckenberg.de ) © 2015 Markus Koch, Johannes Schulz, Gregory Edgecombe.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Koch M, Schulz J, Edgecombe GD (2015) Tentorial mobility in centipedes (Chilopoda) revisited: 3D reconstruction of the mandibulo-tentorial musculature of Geophilomorpha. In: Tuf IH, Tajovský K (Eds) Proceedings of the 16th International Congress of Myriapodology, Olomouc, Czech Republic. ZooKeys 510: 243-267. https://doi.org/10.3897/zookeys.510.8840
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Mandibular mechanisms in Geophilomorpha are revised based on three-dimensional reconstructions of the mandibulo-tentorial complex and its muscular equipment in Dicellophilus carniolensis (Placodesmata) and Hydroschendyla submarina (Adesmata). Tentorial structure compares closely in the two species and homologies can be proposed for the 14/17 muscles that attach to the tentorium. Both species retain homologues of muscles that in other Pleurostigmophora are traditionally thought to cause swinging movements of the tentorium that complement the mobility of the mandibles. Although the original set of tentorial muscles is simplified in Geophilomorpha, the arrangement of the preserved homologues conforms to a system of six degrees of freedom of movement, as in non-geophilomorph Pleurostigmophora. A simplification of the mandibular muscles is confirmed for Geophilomorpha, but our results reject absence of muscles that in other Pleurostigmophora primarily support see-saw movements of the mandibles. In the construction of the tentorium, paralabial sclerites seem to be involved in neither Placodesmata nor Adesmata, and we propose their loss in Geophilomorpha as a whole. Current insights on the tentorial skeleton and its musculature permit two alternative conclusions on their transformation in Geophilomorpha: either tentorial mobility is primarily maintained in both Placodesmata and Adesmata (contrary to Manton’s arguments for immobility), or the traditional assumption of the tentorium as being mobile is a misinterpretation for Pleurostigmophora as a whole.
Evolutionary morphology, head endoskeleton, Myriapoda , skeleto-muscular system, histology
The tentorium of myriapods is a cuticular formation of the head with a distinct composition of exoskeletal bars around the mouth opening and endoskeletal processes (
An immobile tentorium was assumed by
In order to contribute to a clarification of the mobility versus immobility of the tentorium in geophilomorphs, we here present anatomical 3D-reconstructions of the mandibulo-tentorial complex and its muscular system based on histological studies of two species, one representing each of the clades Placodesmata and Adesmata, respectively. Insights obtained demand a more general revision of whether the tentorium in pleurostigmophoran centipedes is mobile at all.
This study is based on histological sections of the head of Dicellophilus carniolensis (Koch, 1847) (Placodesmata, Mecistocephalidae) and Hydroschendyla submarina (Grube, 1792) (Adesmata, Schendylidae). The heads were fixed in alcoholic Bouin solution (modified according to Duboscq-Brazil) after removal of the forcipules, dehydrated in a graded ethanol series, and transferred via propylene oxide into epoxy resin (Araldite). Series of semithin transverse sections (0.5–1 µm thickness) were performed with a Jumbo-Diatome diamond knife on an Ultracut E microtome (Fa. Reichert) and stained with 1% Toluidine blue. Digital images (tiff-format) of the sections were made with an Olympus BX51dotSlide microscope and semi-automatically aligned into a digital image stack with the open source software imodalign (http://www.evolution.uni-bonn.de/mitarbeiter/bquast/software). The image stacks used for 3D-reconstructions (Fig.
Surface model of the mandibulo-tentorial complex, dorsal view onto the left complex within the head capsule (anterior is top). A Dicellophilus carniolensis B Hydroschendyla submarina, tentorial muscles 18 and 22b removed. Numbers refer to muscles as listed in Table
Compilation of all mandibular and tentorial muscles, numbered in accordance to their illustration in Figs
Muscles (this study) | Origin | Insertion | Dicellophilus carniolensis | Hydroschendyla submarina |
Orya barbarica ( |
---|---|---|---|---|---|
Tentorium (tt) | |||||
9 | epicranium | posterior process | + | + | ? (T10) |
14 | clypeus | supramandibular arch | + | + | + (T4/T5, or T2-T6) |
15 | epicranium | supramandibular arch | + |
+ | ? (T7) |
18 | epicranium | supramandibular arch | + | + | ? (T9) |
20 | epicranium | posterior process | + | – | ? (T8) |
22 | forcipular tendon | posterior process | + |
+ | slm / vlm |
Mandible (md) | |||||
3 | epicranium | base | + | + | 26 |
4 | base | gnathal lobe | + | + | 31 |
5 | epicranium | base | + | + | – (25, or 24+25) |
6 | tentorium | gnathal lobe | + | + | 27 |
10 | gnathal lobe | gnathal lobe | – | + | 29 |
12 | tentorium | base | + | + | 22/23 |
13 | epicranium | gnathal lobe | + | + | 20 |
17 | epicranium | base | + | – | 19 (25 fide Manton) |
19 | epicranium | base | + | – (21?) | – |
21 | epicranium | gnathal lobe | – (19?) | + |
21 |
24 | tentorium | base | + | + | – (30, unified with 23 fide Manton) |
26 | mesial inter-connection | base | – | + |
– (32) |
Hypopharynx (hy) | |||||
1 | tentorium | front side along mesial lips | + | + | + |
25 | tentorium | back side near opening of hypoph. gland | + | + | + |
Pharynx (ph) | |||||
8 | tentorium | ventral pharyngeal wall | + |
+ | ? |
Maxilla I (mxI) | |||||
2 | tentorium | coxosternite (paramedial) | + |
+ | (+) |
16 | tentorium | coxosternite (lateral to 2) | + |
– | |
23 | tentorium | coxosternite (paramedial, posterior to 2) | + |
– | |
Maxilla II (mxII) | |||||
7 | tentorium | coxosternite (medial at base of telopodite) | + |
+ | (+) |
11 | tentorium | coxosternite (lateral) | + |
+ |
For three-dimensional reconstructions the software Amira 5.4.5 (FEI Visualization Sciences Group) was used for segmentation. As recommended by
The interactive 3D-mode can be activated by clicking on the images of Figures
Dicellophilus carniolensis, surface model of the left mandibulo-tentorial complex. A Medio-frontal view, tentorial muscle 14 removed; arrow points to condyle of mandibular gnathal lobe B Oblique dorso-frontal view, extrinsic mandibular muscles removed. Numbers refer to muscles as listed in Table
Dicellophilus carniolensis, surface model of the left mandibulo-tentorial complex in situ. Click on the image to activate the interactive 3D-mode. (download 3D model)
Hydroschendyla submarina, surface model of the left mandibulo-tentorial complex. A Medio-frontal view, tentorial muscles 14, 18, and 22b removed as well as hypopharyngeal muscle 25; arrow points to condyle of mandibular gnathal lobe B Oblique dorso-frontal view, extrinsic mandibular muscles 3, 5, and 13 removed as well as tentorial muscles 18 and 22b. Numbers refer to muscles as listed in Table
Hydroschendyla submarina, surface model of the left mandibulo-tentorial complex in situ. Click on the image to activate the interactive 3D-mode. (download 3D model)
In both D. carniolensis and H. submarina the tentorium forms a clasp-like structure dorsally around the mandible (Figs
Dicellophilus carniolensis, selection of micrographs of transverse sections through the head from anterior to posterior. A Section through anterior head part in front of the mandibulo-tentorial complex, highlighting muscles arising from the clypeus B Section through the mandibulo-tentorial complex (left side of head) slightly anterior to C; in the inset (scale: 25 µm) the area of flexibility (arrow) between mandibular gnathal lobe and base is magnified. C Section through the mandibulo-tentorial complex (right side of head) at the level of the cuticular tendon (arrow in inset; scale: 25 µm) of the mandibular gnathal lobe. D Section through posterior part of tentorium and mandible (left side of head), showing collagenous tendon system and mandibular septum. Numbers refer to muscles as listed in Table
The muscular equipment of the tentorium largely corresponds in the two species studied (Figs
Hydroschendyla submarina, selection of micrographs of transverse sections through the head from anterior to posterior. A Section through the anterior head part, showing the mandibulo-tentorial complex at the level of the epipharyngeal bar B Section through the mandibulo-tentorial complex (right side of head) at the level of the junction between epipharyngeal bar and supramandibular arch. C Section through the mandibulo-tentorial complex (left side of head) between the levels shown in B and D. D Section through posterior part of tentorium and mandible (right side of head) at the level of the mesial interconnection of the mandibles by muscle 26. Numbers refer to muscles as listed in Table
Muscles that in Lithobiomorpha and Scolopendromorpha are thought to move the tentorium are represented in D. carniolensis and H. submarina by the following set:
M.9 is a fan-shaped vertical muscle that originates medio-dorsally from the epicranial wall (Figs
M.14 is a broad, fan-shaped muscle passing from the clypeus towards the supramandibular arch of the tentorium to insert on its frontal process and mesial surface along its entire length (Figs
M.15 passes almost transversely from the lateral epicranial wall towards the supramandibular arch, on which it inserts along its dorsal rim on its lateral face. In H. submarina (Figs
M.18 arises medio-dorsally from the epicranial wall and inserts anteriorly on the mesial surface of the posterior process, in front of the insertion of pharyngeal muscle 8 and below the insertion of tentorial muscle 9 (Figs
M.22 is a ventral longitudinal muscle attached to the posterior tip of the tentorial posterior process. In both species the muscle consists of two strands. In D. carniolensis (Figs
In D. carniolensis an additional fan-shaped muscle (M.20) passes from the back of the posterior process anteriorly towards the dorsal epicranium (Figs
The mandibles of D. carniolensis and H. submarina each consist of a rod-shaped base, somewhat twisted at half length, and a gnathal lobe (for SEM-illustration of the latter see
Extrinsic mandibular muscles:
M.3 basically corresponds in the two species in its large extent and transverse orientation. It originates dorso-medially from the epicranial wall and inserts on the dorsal margin of the mandibular base at about half its length (Figs
M.5 is a longitudinal muscle originating dorsally from the posterior wall of the epicranium (Fig.
M.6 arises from the tentorium and passes towards the gnathal lobe. In D. carniolensis this muscle is larger than in H. submarina and shows a more longitudinal course; it originates from the posterior part of the posterior process, where it covers its entire lateral surface, and inserts on the frontal wall of the gnathal lobe (Fig.
M.12 passes from the posterior dorsal margin of the mandibular base towards the supramandibular arch of the tentorium. In D. carniolensis this muscle is larger than in H. submarina, its insertion covering the entire lateral surface of the supramandibular arch from the frontal process towards the origin of the posterior process (Figs
M.13 is a transverse muscle passing from the cranial wall towards the gnathal lobe. In both species it consists of two sections, a larger fan-shaped dorsal section (13a) and a few bundles below it (13b). In D. carniolensis (Fig.
M.17 interconnects the posteriormost end of the mandibular base with the dorso-lateral wall of the epicranium along a (collagenous?) septum connected to the posterior cuticular, non-sclerotized wall of the mandibular gnathal pouch (Figs
M.19 is an almost vertical muscle in D. carniolensis (Figs
M.21 is a slender longitudinal muscle composed of four or five small bundles in H. submarina (Fig.
M.24 interconnects the ventral margin of the mandibular base with the ventral margin of the posterior process. The course of this muscle is almost transverse in H. submarina (Figs
M.26 is a transverse muscle in H. submarina that interconnects the posterior ends of the left and right mandibular bases (Fig.
M.4 is a large muscle in both species, passing from the posterior end of the mandibular base to the dorsal (anterior) wall of the gnathal lobe (Fig.
M.10 is an intrinsic muscle of the gnathal lobe. In H. submarina it connects the lateral distal wall of the gnathal lobe with its proximal, soft mesial wall, immediately in front of mandibular muscle 6 (Fig.
The entire construction of the tentorium surprisingly shows no basic difference between D. carniolensis and H. submarina. They indeed seem to differ only in the spatial extension of the tentorium in correspondence to the different shape of the head, in being relatively broad and short in D. carniolensis versus narrower and more expanded in the longitudinal plane in H. submarina. Previous descriptions of the posterior process (“anterior tentorial apodeme” fide
As inferred from D. carniolensis, the original composition of the tentorium and ancestral arrangement of its cuticular components in Pleurostigmophora are maintained in Placodesmata. A main deviation in Placodesmata concerns the sclerotization of the exoskeletal components that are reduced to slender strips (
There is general agreement on
(i) The original articulation between the tentorium (i.e., its transverse bar) and the cephalic pleurite is maintained in adesmatans but has been transformed into a hinge for the gain of an additional articulation between the tentorium and the labral sidepieces; paralabial sclerites are exceptionally identified in adesmatan species such as Himantarium gabrielis, in which they are no longer articulated to the labral sidepieces but are anteriorly displaced into a ‘non-functional’ position between the cephalic pleurite and the clypeus (
(ii) The lateral shift of the tentorium correlates with a loss of both the tentorial transverse bar and the paralabial sclerites as a result of loss of any tentorial mobility (
(iii) The transverse bar (and its articulation with the cephalic pleurite) is maintained in adesmatans, but it extends straight in line with the epipharyngeal bar, such that the original bifurcation point between these two bars (and their distinct identities) is no longer recognizable. Unified in this manner into a single oblique bar, it positionally replaces the paralabial sclerites, which are lost (
(iv) the paralabial sclerites are fused with the tentorium. Loss of the transverse bar would result in the articulation of the tentorium with the cephalic pleurite via its original articulation with the paralabial sclerites.
The cephalic musculature of H. submarina does not unambiguously allow a choice of any of the four hypotheses (i-iv) on the transformation of the tentorium in Adesmata. The original muscular equipment of the transverse bar in Pleurostigmophora is absent in this species, which may support the view that the transverse bar is absent as well. Absence of these muscles, however, remains inconclusive, because they are also absent in D. carniolensis, in which the transverse bar is unambiguously maintained. The tentorial exoskeleton itself in H. submarina still raises doubts that the tentorium is coalesced with the paralabial sclerite. This is because the sclerotized oblique bar passing from the cephalic pleurite towards the labral sidepiece proved to merely represent the sharp lateral margin of the tentorium, its external surface being mostly inclined into the depth of the preoral cavity (see Koch & Edgecombe, their Fig. 1F). If the oblique bar – which we consider to comprise both the former transverse and epipharyngeal bars – were to include the paralabial sclerite, one would expect it to form a broader surface onto the ventral head wall posterior to the clypeal sclerotization (i.e., outside the preoral cavity).
We accordingly propose that geophilomorphs overall lack any marker to unambiguously recognize paralabial sclerites. Our data favour a loss of paralabial sclerites in the geophilomorph stem species as a simpler assumption than assuming different transformations of these sclerites in Placodesmata and Adesmata. This view implies that the transverse bar and its articulation with the cephalic pleurite are (primarily) maintained in Adesmata.
The basic set of muscles that in non-geophilomorph Pleurostigmophora are thought to move the tentorium proved to be present in D. carniolensis and H. submarina. Among them,
The set of tentorial muscles arising from the dorsal and dorso-lateral wall of the epicranium in lithobiomorphs and scolopendromorphs (T7-T10 fide Manton) is basically maintained in both D. carniolensis and H. submarina, except for muscle T8 (M.20 in this study), which seems to be lost in H. submarina. In both species tentorial muscle 15 deviates from its homologue (T7) in non-geophilomorphs in the shift of its origin towards the lateral epicranial wall, thus acquiring a transverse orientation. Tentorial muscles 9 and 18 deviate from their homologues in non-geophilomorphs (T9 and T10) in the shift of their origin towards a more posterior position, while keeping their distance relative to each other. Compared to D. carniolensis, their greater distance in H. submarina seems to correlate with the stronger longitudinal expansion of the tentorium in this species. The insertion of tentorial muscle 18 (T9) is more derived than in non-geophilomorphs in its expansion onto the mesial surface of the tentorial posterior process. In non-geophilomorphs the corresponding surface of the posterior process mainly serves for insertion of antennal muscles, the insertion of T9 being restricted to the dorsal edge of the posterior process. Its expansion onto the mesial surface in geophilomorphs correlates with the shift of the origin of the respective antennal muscles from the tentorium onto the clypeus.
The arrangement of the clypeo-tentorial, epicranio-tentorial, and ventral longitudinal muscles relative to each other in both D. carniolensis and H. submarina is comparable to a system of six degrees of freedom of movement – its three axes being indicated each by muscles 14 and 22, the set of muscles 9, 18, and 20, and muscle 15, respectively – and basically corresponds to the relative arrangement of their homologues in lithobiomorphs and scolopendromorphs. In applying
A mobile tentorium was already inferred for Placodesmata by
Arguments in support of the former interpretation mainly relate to the strength of the muscles and their apparent arrangement as antagonists for each other. Alternatively, if the tentorial muscles are not used to move the tentorium, their main function may rather be to stabilize the tentorium in suspending it firmly at the cranial wall and to keep it in optimal position for its articulation with the mandibles. This new alternative interpretation gains support from current insights on the tentorium in Adesmata, movements of which have traditionally been denied. A case can further be made to question the view that the tentorium performs swinging movements in Pleurostigmophora as a whole. A considerable bulk of muscles originate from the tentorium: apart from extrinsic mandibular muscles these primarily also include antennal muscles, extrinsic muscles of the first and second maxillae, hypopharyngeal muscles, dilators of the foregut, and suspensory muscles of the collagenous transverse tendon system. These muscles drastically reduce the space available for elaborate movements of the tentorium and, because of their origin from the tentorium, its swinging movements would necessarily have an impact on movements of all these head structures. We further suspect that the original interconnection of the posterior processes of the tentorium by the collagenous transverse tendon system in Pleurostigmophora impedes independent movements of the left and right tentorium, and thus also independent movements of the left and right mandible, if swinging movements of the tentorium are really required for the mandibles. We do not deny that the tentorium is flexible to variable degrees in pleurostigmophorans. This flexibility, however, might not be caused by the need to actively contribute to mandibular movements. To allow the mandibles to act against the tentorium, the latter’s flexibility may rather be attributed to a need to stabilize it.
Our current results for D. carniolensis and H. submarina basically confirm
Among the 14–16 mandibular muscles described for scolopendromorphs (
Mandibular muscle 17 was considered by
Mandibular muscle 26 is remarkable as it seems to represent a remnant of a muscle (32 fide Manton) that in other Pleurostigmophora primarily fills almost the entire concavity of the mandible and interconnects left and right mandible via the transverse mandibular tendon. Its presence in H. submarina (Fig.
The remaining mandibular muscles vary to a lesser degree among geophilomorphs. The strongest adductor of the mandibular gnathal lobe (M.13 in this study; 20 fide Manton) is very much alike in geophilomorphs. As pointed out by
A muscle of the gnathal lobe arising from the dorsal epicranial wall (M.21 in this study and fide Manton) was considered by
The longitudinal muscle (M.12) passing from the tentorium to the posterior end of the mandibular base is remarkably larger in D. carniolensis and O. barbarica than in H. submarina. This may support Manton’s view that originally separate muscles (22, 23, and 33 fide Manton) are primarily unified in geophilomorphs but are partly reduced in H. submarina. The single muscle arising posteriorly from the dorsal epicranial wall to insert at the dorsal margin of the mandibular base (M.5 in this study) may likewise comprise two formerly separate muscles (24 and 25 fide Manton). These assumptions on unifications of muscles, however, remain uncertain, since in scolopendromorphs some of them seem to be variably reduced (according to
Whether these transformations of the mandibular musculature in geophilomorphs alter the mandible mechanism to a degree that movements of the tentorium are dispensable remains unclear. This also considers
Previous arguments for considering the tentorium of geophilomorphs to be immobile are revised as follows:
(1) Derivation of the tentorial skeleton. – Absence of the transverse bar of the tentorium – until now presumed to determine the axis of tentorial swing in Lithobiomorpha and Scolopendromorpha – is rejected for both Placodesmata and Adesmata. In the former, remnants of the collagenous tendon system proved to be preserved. The muscular system of the tentorium remains ambiguous with regards to the fate of the paralabial sclerites. They may be fused to either the labral sidepiece (Placodesmata), or to the transverse bar of the tentorium (Adesmata), but unambiguous evidence for their presence is lacking. Accordingly, paralabial sclerites may have been lost across Geophilomorpha as a whole.
(2) Derivation of the tentorial muscles. – Entire absence of the muscles that are presumed to effect swinging movements of the tentorium in Lithobiomorpha and Scolopendromorpha is rejected for Geophilomorpha. The respective set of muscles is simplified (either by unification or loss), but the main functional groups fide
(3) Derivation of the mandibular muscles. – A simplification of the mandibular musculature is basically confirmed for Geophilomorpha, but
As such, our current insights on the morphology of the mandibulo-tentorial complex in geophilomorphs accordingly cause us to doubt that the mandible mechanism differs among pleurostigmophoran centipedes in terms of whether or not movements of the tentorium are required to abduct the mandibular gnathal lobe. With respect to the apparently immobile tentorium in Scutigeromorpha, the size of the mandible and its armature are inconclusive for this problem. The complexity of the muscles involved renders it difficult to unambiguously reveal their interplay and individual function. We therefore think that kinematic studies of living specimens are required to decisively elucidate the functional role of the tentorium during feeding. For this purpose, current advances in 4D in-vivo microtomography (see, e.g.,
Histological sections for Hydroschendyla submarina were contributed by Liesa Rütjes (Univ. Bonn, Germany). Technical assistance with the digital imagery by Frank Friedrich (Univ. Hamburg, Germany) and Björn Quast (Univ. Bonn, Germany) is gratefully acknowledged. We furthermore thank Lucio Bonato (Univ. Padova, Italy) for discussion of his interpretation of geophilomorph head morphology and three referees for input.
Digital image stack used for 3D-reconstruction of the mandibulo-tentorial complex of Dicellophilus carniolensis
Data type: QuickTime mov file
Explanation note: Series of transverse histological sections from anterior to posterior, provided as movie.
Digital image stack used for 3D-reconstruction of the mandibulo-tentorial complex of Hydroschendyla submarina
Data type: QuickTime mov file
Explanation note: Series of transverse histological sections from anterior to posterior, provided as movie.